SUMMARY

Infrequent and exceptional behaviours can provide insight into the ecology
and physiology of a particular species. Here we examined extraordinarily deep
(300–1250 m) and protracted (>1h) dives made by critically endangered
leatherback turtles (Dermochelys coriacea) in the context of three
previously suggested hypotheses: predator evasion, thermoregulation and
exploration for gelatinous prey. Data were obtained via satellite
relay data loggers attached to adult turtles at nesting beaches
(N=11) and temperate foraging grounds (N=2), constituting a
combined tracking period of 9.6 years (N=26,146 dives) and spanning
the entire North Atlantic Ocean. Of the dives, 99.6% (N=26,051) were
to depths <300 m with only 0.4% (N=95) extending to greater depths
(subsequently termed `deep dives'). Analysis suggested that deep dives: (1)
were normally distributed around midday; (2) may exceed the inferred aerobic
dive limit for the species; (3) displayed slow vertical descent rates and
protracted durations; (4) were much deeper than the thermocline; and (5)
occurred predominantly during transit, yet ceased once seasonal residence on
foraging grounds began. These findings support the hypothesis that deep dives
are periodically employed to survey the water column for diurnally descending
gelatinous prey. If a suitable patch is encountered then the turtle may cease
transit and remain within that area, waiting for prey to approach the surface
at night. If unsuccessful, then migration may continue until a more suitable
site is encountered. Additional studies using a meta-analytical approach are
nonetheless recommended to further resolve this matter.

INTRODUCTION

Deep diving behaviour is well documented for a wide range of air-breathing
marine vertebrates including pinnipeds (e.g.
Le Boeuf et al., 1988;
Sato et al., 2002), penguins
(e.g. Kooyman et al., 1992;
Ryan et al., 2004) and
cetaceans (e.g. Hooker and Baird,
1999; Amano and Yoshioka,
2003). Such behaviours are typically associated with foraging deep
in the water column or at the seabed, yet dives well beyond the usual depth
range (i.e. extraordinary deep dives) are rarely considered explicitly as an
important behavioural component. Nevertheless, it is known that exceptional
behaviours may provide insights into performance maxima for species and reveal
previously hidden aspects of their behavioural ecology. Indeed, infrequent and
extraordinarily deep dives may provide tantalising insights into the ecology
of air breathing marine vertebrates, although establishing the exact role of
such behaviours is not easy as they may occur infrequently and in remote
locations (Boyd, 1999).

Unravelling the function of deep dives in leatherbacks therefore
constitutes a long-standing goal for sea turtle biologists as this exceptional
behaviour has been recorded at tropical breeding grounds for many years (e.g.
Eckert et al., 1986;
Eckert et al., 1989;
Mrosovsky, 1987;
Eckert, 2002;
Myers and Hays, 2006;
Fossette et al., 2008).
Nevertheless, it is difficult to extrapolate behaviours observed throughout
the breeding season to the rest of the year given a distinct behavioural
plasticity whereby diving behaviour changes markedly once turtles move into
open oceanic waters (Hays et al.,
2004a). The opportunity to consider deep dives in this broader
context, however, has been made possible through the development of satellite
relay data loggers (SRDLs; Sea Mammal Research Unit, University of St Andrews,
Fyfe, Scotland) (e.g. Bennett et al.,
2001; Sparling and Fedak,
2004; Hays et al.,
2004a; Biuw et al.,
2007) that convey not just location, but information regarding the
diving behaviour and corresponding environmental conditions via the
Argos network. Utilising this technological advance, we set out to revisit
three specific hypotheses put forward to explain the role of exceptionally
deep dives in this species. (1) Rates of descent between exceptionally deep
and more typical dive events were compared to explore the idea of deep evasive
dives, with further consideration of how the ensuing post-dive recovery
periods at the surface might increase detection by predators. (2) Water
temperatures experienced by leatherbacks during their transit to great depths
were examined to revisit the idea that they may serve some thermoregulatory
function at warmer latitudes. (3) The temporal and spatial patterns of deep
diving during different migratory phases were mapped to examine the potential
benefits of such behaviour for prey detection and acquisition on transit to
principal foraging grounds.

MATERIALS AND METHODS

Instrument deployment

Movements and behaviour of migrating leatherback turtles were determined
using SRDLs. These devices provide information not simply on location but also
on a host of variables including dive depth and water temperature. Twelve
SRDLs were deployed upon leatherback turtles at two sites over 4 years
(Table 1). Three transmitters
were attached to nesting females on Levera Beach, Grenada, West Indies
(12.1°N, 61.7°W) in 2002 with a further eight devices deployed from
the same site in 2003. One transmitter was attached to a female turtle at sea
off the Dingle Peninsula in County Kerry, Ireland (52.24°N, 10.30°W)
in July 2005, with a second transmitter deployed on a male in June 2006
(Table 1).

For all but the 2006 deployment, transmitters were attached to turtles
using a soft harness system (Hays et al.,
2004a; Myers and Hays,
2006). For the 2006 deployment, direct attachment was used
involving drilling three small holes through the median dorsal ridge. A
transmitter glued to a highly streamlined catamaran-style base plate (designed
to sit either side of the ridge) was attached using biodegradable, plastic
cable ties that were passed through the holes. For a full description of this
method see Doyle et al. (Doyle et al.,
2008).

Dive data

Owing to the limited bandwidth of the Argos system, depth was relayed to an
accuracy within 2 m for dives to 65 m, and within 4 m for dives between 65 m
and 128 m, decreasing to ∼30 m for dives >500 m [see Myers et al. for a
validation of dive profiles relayed via the Argos satellite system
(Myers et al., 2006)]. Using
bespoke software, these depth data were analysed onboard the SRDL prior to
transmission. Data for individual dives were generated when the depth exceeded
10 m. Start times for dives were determined by salt-water switches on the SRDL
that perceived the transmitter was fully submerged, with the end of the dive
defined when the transmitter again broke the surface or a depth <2 m was
recorded. To account for drift in the recording of depth values, SRDLs perform
a zero-point calibration on-board by re-setting their internal zero-offset
whenever the saltwater switch detected that the device was at the surface,
i.e. ensuring that a depth of zero metres is recorded for this time
(Myers and Hays, 2006).

Once a dive was completed, onboard software examined the dive profile and
determined the time and depth of the five most prominent points of inflection
during the dive. The time and depth of these five points, together with the
time of the end of the dive and dive duration were then transmitted. To ensure
effective transmission of data, information for each dive was stored within a
buffer on the SRDL so that it would be transmitted randomly for the next 10
days. In this way, the specific dive profiles obtained via the Argos
system were not simply a function of the surfacing behaviour of the turtle
immediately subsequent to each dive (Hays
et al., 2004a). A dive number accompanied the depth and time data
for each dive, so that it was possible to determine the number of dive
profiles that were not received via Argos.

In conjunction with data for individual dives, a summary of all dive
information for 6h periods was also generated by each SRDL. Each summary
period contained data for a range of parameters including (1) percentage of
time spent at the surface (i.e. saltwater switch was dry for longer than 10
min); (2) percentage of time spent shallower than 10 m; (3) percentage of time
spent deeper than 10 m; (4) mean depth of dives to over 10 m; (5) mean dive
duration for dives to over 10 m; and (6) maximum depth attained. Although
SRDLs include a speed sensor, this always rapidly clogged and ceased to
function, so these limited data are not considered here.

Classification of deep dives

A frequency histogram of maximum dive depth was constructed for all dives
recorded by each turtle combined (N=26,146 dives;
Fig. 2). Data were broken down
into 100 m depth bins, revealing that 99.6% of all dives (N=26,051)
were to depths <300 m with only 0.4% (N=95) extending to greater
depths. In this paper the term `deep dives' therefore refers to all dive
events >300 m (Fig. 2).

Determining local time of sunrise and sunset

The time of each deep dive was converted from GMT to local time by using
the interpolated longitude for where each dive occurred. Day length and the
time of sunrise and sunset (i.e. when the sun was at zero degrees elevation)
were calculated for the interpolated position of each dive using bespoke
online software
(http://www.csgnetwork.com/sunriseset.html).

Determining vertical rate of descent during deep dives

Vertical descent rate was calculated from the five points of inflection
assigned to each dive profile. This was achieved in two ways. First, the depth
of the first point of inflection (D1) was divided by the
time it took the turtle to reach this depth (T1). However,
the first point of inflection can occur at varying stages along the descent
phase and may therefore not be consistently representative of the overall
vertical rate of descent down to the maximum depth. A second approach was
therefore also adopted whereby the deepest point of inflection
(Dmax) was divided by the corresponding time it took to
reach this depth.

Frequency histogram of all dives completed by the 13 turtles combined,
where maximum depth data were available (N=26,146 dives).

Temperature data

A detailed description of how SRDLs measure water temperature is given in
McMahon et al. (McMahon et al.,
2005). Temperature and depth (pressure) were sampled at 1 Hz, and
the results averaged into 1 dbar bins (1 dbar increase in pressure being
equivalent to 1 m of seawater; 1dbar is 10kPa). Twelve depth–temperature
points were obtained for each profile.

Overview of dive data

The following generic data for the 13 tracked turtles are given in
Table 1: (1) total number of
dives recorded; (2) maximum depth; (3) number of deep dives recorded; (4)
percentage of all recorded dives >300m; and (5) mean depth of all dives.
From a total of 26,145 individual dives recorded, 4949 were <10 m, which is
below the threshold at which points of inflection are recorded during dives.
For these dives only maximum depth data are available. For the 21,196 dives>
10 m the mean maximum dive depth for all animals combined was 52.9 m
(s.e.m., 0.35 m). The deepest dive, to 1250 m, was conducted by turtle 13, the
large male tracked from County Kerry in Ireland on 30 December 2006
(18.58°N, 25.79°N). To further ascertain whether our proxies of
descent rate (i.e. rate to D1 and
Dmax) were appropriate for all dives >10 m, we plotted
each profile in turn (N=21,196 dives) prior to analysis. This
revealed a marked uniformity in the shape of the dive profiles (i.e. they were
of a similar V-shaped profile with brief bottom times and direct descent and
ascent phases) rendering the classification of dives into different profile
types (e.g. Houghton et al.,
2002; Reina et al.,
2005) unnecessary. Interestingly, the distinct U-shaped dive
profiles detailed by Reina and colleagues (attributed to brief periods of sea
bed resting) were not identified during this preliminary analysis
(Reina et al., 2005). This is
perhaps understandable as this previous study suggested this unusual
leatherback behaviour reflected the constrained bathymetry surrounding their
study site.

Vertical rate of descent and duration of deep dives

To test for irregularities in deep-diving behaviour that may be indicative
of periodic threats or predator evasion, the rate of descent was determined
for all dives where five points of inflection were recorded (N=20,497
dives). Significant, yet weak, linear relationships were found between maximum
dive depth and the rate of descent to D1
(F1,20496=0.001, r2=0.26,
P<0.0001) and Dmax
(F1,20496=2391, r2=0.09,
P<0.0001). To further elucidate these two relationships, data were
classified into 100 m bins of dive depth (e.g. 0–100 m, 101–200 m)
and mean rates of descent were calculated
(Fig. 3). The midpoint of each
depth bin (e.g. 50 m, 150 m) was then plotted against the mean rate of descent
for that bin, revealing highly significant log-normal relationships for
descent to D1 (F3,5=23.11,
r2=0.93, P<0.0001;
Fig. 3A) and
Dmax (F3,5=121.78,
r2=0.98, P<0.0001;
Fig. 3B).

Next, to test whether a slower vertical rate of descent during deep dives
manifested itself in an increased duration, mean durations (±1 s.d.)
were determined for each of the 100 m depth bins used to derive vertical
descent rates (Fig. 3C).
Bradshaw and colleagues (Bradshaw et al.,
2007), working from the same SRDL data set, used the maximum
duration of dives at different depths to infer the aerobic dive limits (ADL),
defined by Kooyman and colleagues as the dive duration beyond which blood
lactate levels begin to rise above resting levels
(Kooyman et al., 1980). The
mean maximum ADL for the nine leatherback turtles considered was
37.6±6.1 min (c.v., 16%) and ranged from 19.2 to 48.1min
(Bradshaw et al., 2007). This
maximum ADL is shown on Fig.
3C, revealing that dives >800 m appear to be anaerobic, yet
dives between 300 and 800 m largely fall within the aerobic diving
capabilities for the species. The accumulation of lactate resulting from
anaerobic respiration requires an air-breathing diver to spend time recovering
at the surface between long dives
(Thompson and Fedak, 1993),
and this is expressed as a positive relationship between dive duration and
post-dive surface intervals (Costa et al.,
2001). SRDLs provide numerous measures of diving behaviour (for
details, see Hays et al.,
2004a; McMahon et al.,
2007), but not all consecutive dive profiles are measured. Where
data were available, therefore, we reconstructed dive profiles leading up to
and following deep dives greater than 800m and the inferred maximum ADL of
48.1min (where data were available N=5 dives;
Fig. 4). As suspected, each
deep dive was followed soon after by a prolonged post-dive surface interval
(mean, 2.1±0.85h; maximum, 2.61h; minimum, 1.04h) supporting the
inference that such events are anaerobic
(Fig. 4C). These times at the
surface could represent resting or might possibly encompass periods of
extremely shallow swimming (Eckert,
2002). Nonetheless, the salient point remains that repeated bouts
of diving beyond 2m were not evident for protracted periods of time following
anaerobic dives, with the overall inference that oxygen debts needed to be
repaid.

Temperatures experienced during deep dives

It has previously been suggested that diving behaviour may serve some
thermoregulatory function in leatherback turtles
(Paladino et al., 1990;
Wallace et al., 2005;
Southwood et al., 2005). To
assess the range of temperatures experienced by leatherback turtles during
rare and exceptional deep dives (>300 m), we examined the
temperature–depth data from the SRDLs. To avoid issues of inter-annual
variation we considered data for the 2003 Grenada deployments in isolation. In
total, temperature–depth records were available for 1544 dives between 4
and 52°N. Unfortunately a software malfunction within the on-board
software coded all data from depths >500 m as a single value of 500 m,
rendering all data in excess of this depth invalid (i.e. analysis could only
be conducted for data <500 m). Once this error had been taken into account,
valid temperature–depth data were available for 147 dives >300 m but<500 m. Examples of nine temperature profiles from increasing latitudes are
given in Fig. 5A, revealing
that, independent of latitude, water temperature typically decreases very
slowly below 350 m. Using the power relationships derived from each profile,
predictions of water temperature at 50m intervals were made. The rate of
thermal change through the water column (ΔT) was determined as
the decrease of temperature within a 50 m depth band, confirming that, in each
case, the rate of temperature decrease slowed significantly below 350 m
(Fig. 5B).

(A) Mean (±1 s.d.) vertical rate of descent to the first point of
inflection (D1) for all turtles combined, classified into
100 m depth bins (N=22,085 dives); (B) mean (±1 s.d.) vertical
rate of descent to the deepest point of inflection (Dmax)
for all turtles classified into 100 m depth bins (N=21,196 dives).
For both parts of the figure all data are from dives displaying five points of
inflection. (C) Dive depth versus dive duration for dives where data
were available (N=21,196 dives). Dotted line shows maximum inferred
aerobic dive limit (ADL) for leatherbacks
(Bradshaw et al., 2007).

Temporal patterns in deep-diving behaviour

The timing of deep-diving events was converted from GMT to local time,
revealing a normal distribution (Kolmogorov–Smirnov test,
P=0.07) in daily time of occurrence. A Gaussian 3-parameter curve was
then fitted, revealing a peak in occurrence just after midday
(F2,20=63.93, r2=0.86,
P<0.0001; Fig.
6).

Spatial patterns in deep-diving behaviour

Deep dives were recorded throughout the entire North Atlantic Ocean
(Fig. 7A). The greatest number
of deep dives recorded for an individual turtle was 24 (turtle 8), with a
minimum of 0 recorded for three individuals (turtles 2, 11 and 12), although
turtle 11 was only tracked for a period of 2days
(Table 1). The apparent
weighting of deep dives towards lower latitudes reflects the bias of data
towards the Caribbean and proximate tropical Atlantic given that 11 of the 13
turtles were tracked from Grenada. This is compounded by the fact that
post-nesting females may only reach the more productive waters of the northern
Atlantic during the autumn months when decreasing water temperatures or
shifting prey fields may truncate their residency and drive the animals
further south (Ferraroli et al.,
2004; Houghton et al.,
2006a; McMahon and Hays,
2006). To account for this bias, deep dive data were normalised by
taking into account the number of dive profiles recorded within different
4° latitudinal bands (e.g. 4.00–7.99°N;
Fig. 7B). This revealed a
highly significant log-normal relationship showing that deep dives were not
uniformly distributed throughout the northern Atlantic with a peak occurring
between 15 and 30°N (F2,11=31.64,
r2=0.88, P<0.0001).

(A) Each profile represents temperature data gathered from an individual
turtle during a single dive. Data are given in raw format to demonstrate how
profiles varied with latitude (marked in the key to the side of the figure).
(B) Rate of temperature change (ΔT, °C) at 50 m depth
intervals based upon power relationships derived from the temperature profiles
given in A.

Frequency distribution of all dives >300 m (N=95) revealing a
peak in occurrence just after midday.

Deep diving during different phases of migration

`Distance from home' data (i.e. distance from the deployment site) were
plotted against time for all post-nesting turtles leaving their breeding
grounds in the Caribbean (Fig.
8). Unfortunately, for two turtles (turtles 4 and 5;
Table 1) these data were
incomplete and were therefore excluded from the analysis. Additionally, the
male and female turtles tracked from Dingle (turtles 12 and 13) were not
included as their stage within the 2–3 year reproductive cycle was not
known, rendering comparison with post-nesting individuals impossible. For the
six remaining turtles, post-nesting migrations were divided into four separate
phases: (1) the internesting interval (i.e. movements within the Caribbean
between subsequent nesting events); (2) the transit phase (i.e. movements from
breeding to foraging sites in the northern or eastern tropical Atlantic); (3)
the resident phase (signified by the end of the transit phase at which point
individuals remain for protracted periods within specific oceanic or coastal
areas); and (4) the post-residence phase (i.e. movements away from residence
areas). These phases were defined using a simple criterion for distance from
home. For example, internesting intervals were defined as the time from
transmitter deployment to the time the female left the Caribbean after her
last nest. The transit phase began once the female had left the Caribbean
until a time when the distance from home slowed to a rate of <50 km per
week for two consecutive weeks. Once this minimum threshold was passed the
turtle was said to be `resident' in temperate waters. The post-residence phase
was taken to begin once movements south were again >50 km per week for two
consecutive weeks. Although this method captures the distinct phases of
migration well, more robust analyses using switching state–space models
are required for future studies (Jonsen et
al., 2007). To assess how deep-diving behaviour varied between
different phases of the migration, the maximum depths recorded during 6h
summary periods were plotted against time and distance from home
(Fig. 8). Next, the proportion
of 6h periods with a maximum depth >300 m was determined for each turtle
during each phase of the migration and arc-sin transformed. Data for both the
internesting interval and transit phase were only available for three turtles
(turtles 7, 8 and 9) as transmitters were deployed on the remaining turtles
during their last nesting event of the season so that they commenced transit
directly after re-entering the water. Student's t-tests revealed a
slight increase in the number of deep dives during transit when compared with
the internesting interval (t=–2.25, P>0.05).
However, it should be noted that this behaviour was quite common during the
internesting period. A more distinct behavioural shift was evident between
transit and residence, with a significant decrease in the proportion of deep
dives at the end of the transit period (t5=4.67,
P=0.002; Fig. 8). No
such difference was detected between the residence and post-residence phases,
although deep dives were recorded during the latter for two of the six
turtles. Lastly, the proportion of deep dives was greater during transit than
in the post-residence phase (t5=2.69, P<0.05),
although this was possibly a function of insufficient data for the latter as a
result of decreasing transmitter efficiency with time.

(A) Spatial pattern of deep dives (>300 m) throughout the North
Atlantic. Data from individual depth profiles are shown as open circles
(N=97 dives). On occasion a maximum depth >300 m would be recorded
in the summary data without an actual profile being recorded. To account for
these events, all summary periods with maximum depths >300 m are shown as
open triangles (N=147 periods). (B) The occurrence of deep dives as a
proportion of the total number of dives recorded at different latitudes
(combined into 4° bins). Data are given as mid-points for 4° latitude
bins. The decreased occurrence of deep dives between 4.00 and 7.99°N
should be interpreted with caution as data were only available for these
latitudes from three of the 13 turtles.

DISCUSSION

The principal challenge for many migratory species is often how to cross
large areas, such as deserts and oceans, without a suitable habitat for
refuelling (Klasson, 1996).
Such problems of prey availability may be further compounded by an increased
risk of predation or exposure to sub-optimal environmental conditions, each in
turn applying its own evolutionary pressure to the migrant. This scenario is
clearly demonstrated by leatherback turtles, which often spend the greater
part of any reproductive year transiting between jellyfish-rich temperate
foraging grounds (Houghton et al.,
2006a; Eckert,
2006; James and Herman,
2001) and jellyfish-poor nesting sites in tropical regions
(James et al., 2005a,
James et al., 2005b). Within
this behavioural framework, the exact role of deep dives remains
intriguing.

The maximum depth recorded in 6h summary periods for the entire tracking
period are given for six turtles tracked from Grenada in 2002 and 2003 (PTT
number given on individual figures). Depths <300 m are shaded on each
figure to help identify deep dives according to our classification. Distance
from home (i.e. Grenada) is also given on the secondary y-axis and
denoted by a solid line. Time is classified into different stages of
migration, which can be observed from changes in the distance from home data:
II, internesting interval; TP, transit period; RP, residence period; PRP,
post-residence period.

Predator avoidance

One of the earliest explanations put forward was that leatherbacks dive
deeply to evade predators encountered en route. Certainly, they may
be attacked by sharks (Keinath and Musick,
1993) or killer whales (Orcinus orca) around breeding
sites in the Caribbean and whilst foraging in the northeast Pacific
(Caldwell and Caldwell, 1969;
Pittman and Dutton, 2004).
However, Cropp documented essentially surface evasive behaviour in a
leatherback turtle in the presence of a white shark, Carcharadon
carcharius (Cropp, 1979).
This included erratic diving, rolling at the surface and violent flailing of
the turtle's flippers as it floated on its back. Even though this anecdotal
evidence suggests that leatherbacks may not immediately dive to avoid
predators, there is certainly a vertical and thermal overlap in range between
white sharks and leatherbacks [adults recorded to depths of 980 m in waters as
cold as 3–4°C (Bonfil et al.,
2005)], although such studies of this predator in the Atlantic are
currently lacking. Nevertheless, questions regarding evasive deep-diving
behaviour in marine reptiles extend back much further than extant species,
with Motani and colleagues speculating that ichthyosaur genera, with poor
visual acuity at depth, may have contracted the bends during exceptionally
deep predator avoidance dives (Motani et
al., 1999). Extrapolating this idea to the present, there is some
scope for suggesting that exceptionally deep dives in leatherback turtles may
also reflect a periodic and exceptional predator avoidance response,
especially as high partial pressures of carbon dioxide in the blood (through
departure from normal diving patterns) have been recorded for sea turtles
(Rothschild, 1991). However,
our data suggest that this is not the case here. For example, during an
evasive dive the vertical descent rate should logically be in excess of more
typical behaviours within shallower waters (i.e. travelling or foraging
dives), yet turtles appear to descend at a reduced rate for dives greater than
600m (Fig. 3B). Additionally,
the physiological demands of pushing beyond the ADL appear to require
substantial pre-dive preparatory and post-dive recovery periods at the surface
(Costa et al., 2001)
(Fig. 4) that would do little
to alleviate the risk of predation. Although the exact nature of these
post-dive surface (or near-surface) events is difficult to define, owing to
the issues of resolving dive events <2 m (Eckert et al., 2002;
Myers and Hays, 2006), an
overall reduction in diving activity is clearly evident after deep dives. This
may reflect one of the two strategies used by reptiles to reduce overall
metabolic demands during periods of moderate to severe hypoxia
(Hicks and Wang, 2004).
Firstly, they can use behavioural reductions in preferred body temperature
that, through the direct effect of temperature on biochemical processes (the
`Q10 effect'), decreases the aerobic demands of the tissues.
Secondly, at a constant body temperature, animals can actively down-regulate
ATP demands (Hicks and Wang,
2004). So whether breathing at the surface or remaining fairly
inactive in the top 2 m, the proposition that extremely deep dives elicit a
metabolic and behavioural response in leatherbacks remains valid.

Some consideration must also be given to the possibility that leatherbacks
dive to shed the transmitters themselves, which under natural scenarios might
represent behaviour to dislodge commensal or parasitic species such as remoras
(Echeneis spp.). This seems unlikely, however, as leatherbacks with
only small time–depth recorders wired onto flipper tags have also been
shown to exhibit deep-diving behaviour
(Myers et al., 2006).
Moreover, the inability of other turtle species to dive deeply, which may be
prone to commensal organisms during oceanic transit phases (e.g. green turtles
moving between Brazil and Ascension Island), suggests that this factor alone
would be insufficient to explain the deep-diving behaviour described here.
This reservation also extends to the documented behaviour of female sea
turtles diving to dislodge male turtles during mating attempts
(Reina et al., 2005). Although
turtles clearly employ this strategy to avoid unwanted attention close to
nesting sites (where mating takes place), the predominance of deep dives
during post-reproductive migrations suggests this factor cannot explain the
majority of such events.

Thermoregulation

The physiological adaptations of leatherback turtles (including low
metabolic rate, large thermal inertia, blood flow adjustments and peripheral
insulation) allow them to maintain elevated body temperatures in cold water
and avoid overheating in the tropics
(Paladino et al., 1990;
Southwood et al., 2005;
Wallace et al., 2005). The
combined inference from previous studies is that leatherback turtles with
increased activity levels (through nesting behaviour) might avoid overheating
by increasing the proportion of time spent in cool waters, thus behaviourally
moderating their body temperature by using cooler water as a heat sink
(Paladino et al., 1990;
Southwood et al., 2005;
Wallace et al., 2005). In
support of this concept, it has been shown that leatherback turtles spend the
highest percentage of time in cooler waters in the early third of the
internesting period, implying that increased heat loads incurred during
nesting require shuttling to colder, deeper waters
(Wallace et al., 2005).
Therefore, could exceptionally deep dives be simply extreme examples of this
cooling behaviour? Fig. 5B
indicates that this is probably not the case as temperature decreases at a
negligible rate below 350m, implying that the opportunities to shed heat to
the external environment would be only fractionally better deep in the water
column (e.g. ≥800m) than at more moderate depths (300–400m), and
would incur far greater transport costs. However, given the importance of swim
speeds to metabolic rate, and thus heat generation (e.g.
Southwood et al., 2005;
Bostrom and Jones, 2007), this
finding alone is not conclusive. Unfortunately, as the SRDL speed sensors all
failed soon after deployment (presumably through impeller clogging), it was
not possible to conduct any analysis of directly measured swim speeds. This
behavioural component should therefore be incorporated into future
investigations of deep diving to thoroughly resolve the issue of their
thermoregulatory potential. Moreover, such investigations should include
direct measurements of leatherback body temperatures, dive behaviours, water
temperatures, metabolic rates and blood flow simultaneously to provide the
basis of an integrated bio-energetic model
(Wallace and Jones, 2008).

Prey detection and acquisition

Attempts to locate prey might explain the decreased descent rate of dives>
600 m, with turtles possibly surveying the water column as they descend.
Certainly, for leatherbacks the occurrence of deep dives during the daytime
supports the notion of speculative excursions in search of gelatinous
zooplankton within the deep scattering layer
(Eckert et al., 1989;
Hays et al., 2006). This
biological stratum comprises a wide range of potential prey items including
siphonophores, salps and pelagic medusae
(Barham, 1963;
Barham, 1966;
Michel and Foyo, 1976;
Roe et al., 1984) that are
often concentrated below 600 m during the day and move near the surface at
night in response to diminishing light levels
(Backus and Clarke, 1964;
Eckert et al., 1989).
Consequently, the idea that feeding, or attempted feeding
(Myers and Hays, 2006;
Fossette et al., 2008), takes
place predominantly at night when prey are far more accessible is gaining
acceptance (e.g. Eckert et al.,
1989; Hays et al.,
2004a; Hays et al.,
2006; Jonsen et al.,
2007). Put differently, the transit costs associated with deep
daytime feeding may simply be too expensive as the gelatinous prey of
leatherbacks would offer a minimal payback
(Doyle et al., 2007). This
notion of night-time feeding is supported by the visual adaptations of
leatherbacks such as the concentration of ganglion cells in the superior
temporal portion of the retina called the area temporalis. It is thought that
leatherbacks probably use this concentrated area of visual cells to spot
gelatinous zooplankton in the water column below them
(Oliver et al., 2000).
Additionally, it has been suggested that leatherbacks may use the
bioluminescence of certain deep-sea gelatinous zooplankton, such as pyrosomes,
to assist with locating suitable prey items
(Davenport and Balazs, 1991).
However, this suggestion prompts the question that if leatherbacks are
perfectly capable of finding prey in low light levels, why do they simply not
look for suitable patches at night, negating the requirement to dive to
extreme depths during the day? The possible answer may relate to the dichotomy
within leatherback diving behaviour whereby repeated dives to potential
foraging sites occur during the night and extended periods of travelling occur
during the day (Hays et al.,
2004a; Hays et al.,
2004b). Thus, the decisions of whether or not to keep moving or
stay in a particular area need to be made during periods of transit (i.e.
daylight hours) if leatherbacks are to maximise their rate of travel to more
productive temperate waters. Although not ideal, the predominance of deep
dives around midday certainly suggests that leatherbacks may make the best of
a bad job by searching for prey when ambient light levels throughout the water
column are at their greatest.

The notion of deep speculating dives during the internesting season comes,
however, with a major caveat as it has been suggested that feeding may be
suppressed in gravid sea turtles (Owens,
1980). This theory was indirectly supported by Reina and
colleagues who integrated time–depth recorder data and video footage to
investigate leatherback internesting behaviour in Pacific Costa Rica
(Reina et al., 2005). During
this study potential prey items such as scyphozoan jellyfish, ctenophores and
salps in aggregations or singly were observed in the turtle's field of view at
least once per hour in all deployments but there were no visible indications
of feeding activity. Alternatively, recent studies using beak-opening sensors
have provided good, yet indirect, evidence to suggest that attempts to feed
are indeed made, although further work to resolve feeding from drinking events
are required (Myers and Hays,
2006; Fossette et al.,
2008). Nevertheless, even if we accept that the issue of
internesting foraging is unresolved, the key point remains that deep dives
occur predominantly during transit to foraging grounds (where dietary
suppression should not come into effect), yet cease to occur once the
individual enters the residence stage (Fig.
8). This pattern is consistent with previous studies of migrating
leatherbacks, which revealed a more generic shift between deeper, longer dives
during transit (Jonsen et al.,
2007; Reina et al.,
2005) and extended periods of very shallow dives at high latitudes
(Hays et al., 2006). Most
probably, this behavioural plasticity represents a change in available prey
from mid-water gelatinous zooplankton such as salps, siphonophores and
pyrosomes during transit [found at 500–700 m during the day, rising to
the top 100 m at night (Angel and Pugh,
2000)], to surface aggregations of medusae (e.g. Cnidaria:
Scyphozoa) within temperate and coastal waters
(James and Herman, 2001;
Houghton et al., 2006a;
Houghton et al., 2006b;
Witt et al., 2007). Bringing
all this evidence together, we therefore suggest that infrequent,
exceptionally deep, daytime dives allow leatherbacks to assess whether
adequate (nocturnally ascending) prey are present at depth and are not
foraging dives in their own right.

Viewed in a migratory context, our findings suggest that if suitable
resources are encountered during a deep dive then the turtle may cease transit
and remain within that area, waiting for prey to approach the surface at
night. If unsuccessful, then migration may continue with deep dives being
employed periodically to assess the water column. This idea is compliant with
the findings of Doyle and colleagues who recorded the long-term residence (76
days) of a leatherback within a meso-scale feature in the temperate north east
Atlantic (Doyle et al., 2008).
Upon leaving this inferred `prey patch' there was a distinct change in the
turtle's behaviour characterised by numerous deep dives (>500 m) over a 2
week period. Whether foraging conditions had deteriorated or the turtle had
simply wandered out of a suitable patch is unknown, yet once the period of
deep-diving behaviour ended the turtle began to move south at a significant
rate (67.2 km day–1) implying a decision to abandon searching
for prey at high latitudes.

To conclude, leatherback turtles appear not to fit the general model of
migration when responses to prey are suppressed during transit
(Hays et al., 2006), but
operate as `income breeders' (Jonsson,
1997) supplementing their existing reserves en route
until some threshold prey abundance is surpassed. Within this context, deep
exploratory dives appear to play an important role in prey location,
particularly during periods of extensive transit. However, further studies are
required to address this theory, perhaps through a meta-analytical approach
combining information on deep dives from leatherbacks at different geographic
locales. Further empirical data are also required on the mid- and deep-water
prey fields available to leatherback turtles so that the potential rewards of
exploratory deep dives can be more clearly defined. For example, if
leatherback turtles were merely adapted to feed upon epipelagic jellyfish
aggregations found at temperate latitudes, then the evolutionary pressure
would lie in getting back to such areas as quickly and efficiently as possible
and not in the ability to dive to great depths. Furthermore, as leatherbacks
spend significant time away from temperate shelf waters, where the abundance
of jellyfish medusae is greatest, it seems evident that mid-water prey may
form a more integral part of their diet than once thought.

LIST OF ABBREVIATIONS

ADL

aerobic dive limit

D1

depth to first point of inflection during dive descent

Dmax

depth to deepest point of inflection during dive descent

T1

time to first point of inflection during dive descent

Tmax

time to deepest point of inflection during dive descent

GMT

Greenwich mean time

PTT

platform terminal transmitter

SRDL

satellite relay data logger

ΔT

rate of temperature change (°C)

ACKNOWLEDGEMENTS

Caribbean SRDL deployments were supported by grants to G.C.H. from the
Natural Environment Research Council of the UK (NERC) and the Marine
Conservation Society of the UK (MCS). We thank the Grenadian Ministry of
Agriculture, Forestry, Land and Fisheries and Ocean Spirits Inc. for
permission to conduct this work and generous support in the field. Irish SRDL
deployments were funded by a European Regional Development Fund (INTERREG
IIIA) grant to G.C.H. and J.D. and by The Irish Marine Institute and National
Parks and Wildlife Service, Ireland. We also extend sincere thanks to Mara Beo
Oceanworld Aquarium and Pádraig Frank O'Súllibháin
without whom the tagging programme in Ireland would not have been possible.
Finally, we are extremely grateful to the two reviewers who substantially
improved the quality of this manuscript.

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